Rehabilitation treatment of gait in patients with Parkinson's disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training.

Abstract

Freezing is a disabling symptom in patients with Parkinson's disease. We investigated the effectiveness of a new rehabilitation strategy based on treadmill training associated with auditory and visual cues. Forty Parkinsonian patients with freezing were randomly assigned to two groups: Group 1 underwent a rehabilitation program based on treadmill training associated with auditory and visual cues, while Group 2 followed a rehabilitation protocol using cues and not associated with treadmill. Functional evaluation was based on the Unified Parkinson's Disease Rating Scale Motor Section (UPDRS III), Freezing of Gait Questionnaire (FOGQ), 6-minute walking test (6MWT), gait speed, and stride cycle. Patients in both the groups had significant improvements in all variables considered by the end of the rehabilitation program (all P = 0.0001). Patients treated with the protocol including treadmill, had more improvement than patients in Group 2 in most functional indicators (P = 0.007, P = 0.0004, P = 0.0126, and P = 0.0263 for FOGQ, 6MWT, gait speed, stride cycle, respectively). The most striking result was obtained for 6MWT, with a mean increase of 130 m in Group 1 compared with 57 m in Group 2. Our results suggest that treadmill training associated with auditory and visual cues might give better results than more conventional treatments. Treadmill training probably acts as a supplementary external cue.

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Rehabilitation Treatment of Gait in Patients with Parkinson’s
Disease with Freezing: A Comparison Between Two Physical
Therapy Protocols Using Visual and Auditory Cues with or
Without Treadmill Training
Giuseppe Frazzitta, MD,1* Roberto Maestri, MD,2Davide Uccellini, MD,3
Gabriella Bertotti, MD,1and Paola Abelli, MD1
1Department of Physical Therapy, Scientific Institute of Montescano, S. Maugeri Foundation IRCCS, Montescano, Italy
2Department of Biomedical Engineering, Scientific Institute of Montescano, S. Maugeri Foundation IRCCS, Montescano, Italy
3Department of Neurology, Tradate Hospital, Varese, Italy
Abstract: Freezing is a disabling symptom in patients with
Parkinson’s disease. We investigated the effectiveness of a
new rehabilitation strategy based on treadmill training asso-
ciated with auditory and visual cues. Forty Parkinsonian
patients with freezing were randomly assigned to two
groups: Group 1 underwent a rehabilitation program based
on treadmill training associated with auditory and visual
cues, while Group 2 followed a rehabilitation protocol using
cues and not associated with treadmill. Functional evaluation
was based on the Unified Parkinson’s Disease Rating Scale
Motor Section (UPDRS III), Freezing of Gait Questionnaire
(FOGQ), 6-minute walking test (6MWT), gait speed, and
stride cycle. Patients in both the groups had significant
improvements in all variables considered by the end of the
rehabilitation program (all P = 0.0001). Patients treated with
the protocol including treadmill, had more improvement than
patients in Group 2 in most functional indicators (P 5
0.007, P 5 0.0004, P 5 0.0126, and P 5 0.0263 for FOGQ,
6MWT, gait speed, stride cycle, respectively). The most
striking result was obtained for 6MWT, with a mean
increase of 130 m in Group 1 compared with 57 m in Group
2. Our results suggest that treadmill training associated with
auditory and visual cues might give better results than more
conventional treatments. Treadmill training probably acts as
a supplementary external cue. ? 2009 Movement Disorder
Society
Key words: Parkinson’s disease; freezing; rehabilitation;
treadmill training
Parkinson’s disease is a neurodegenerative disorder
due to the depletion of dopamine in the basal ganglia,
with progressive reduction in the speed and amplitude
of movements. Freezing of gait is a disorder in which
patients are unable to initiate or continue locomotion.
This phenomenon is frequent in patients with Parkin-
son’s disease and can be very disabling because it
impairs mobility and restricts independence. Freezing
is one of the causes of falls in patients with Parkin-
son’s disease and occurs in various situations: when
starting to walk, during turning, when approaching a
narrow space, and just before reaching destination.
The freezing phenomenon is very difficult to treat.
The pharmacological treatment is usually disappointing:
whereas patients with freezing in ‘‘off’’ states can gain
benefit from an increase in levodopa dosage, this was not
observed in patients with freezing in ‘‘on’’ states.1,2
Rehabilitation is a possible treatment for gait disor-
ders in patients with Parkinson’s disease. Many studies
have shown the efficacy of rehabilitation at improving
specific impairments and functional limitations in indi-
viduals with Parkinson’s disease. In particular, they
have shown the efficacy of auditory (musical beats)
and visual (white lines) cues.3-7Treadmill training,
with or without partial body-weight support, also
seems promising in the restoration of gait patterns.8-10
Potential conflict of interest: None reported.
Received 20 December 2008; Accepted 15 January 2009
Published online 15 April 2009 in Wiley InterScience (www.
interscience.wiley.com). DOI: 10.1002/mds.22491
*Correspondence to: Dr. Giuseppe Frazzitta, Department of Physi-
cal Therapy, Scientific Institute of Montescano, S. Maugeri Founda-
tion IRCCS, Via per Montescano, 27040 Montescano (PV), Italy.
E-mail: miangiu@yahoo.it
1139
Movement Disorders
Vol. 24, No. 8, 2009, pp. 1139–1143
? 2009 Movement Disorder Society

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However, there are no published studies on the use of
treadmill training in association with auditory or visual
cues. We, therefore, developed a rehabilitation protocol
for gait disturbances and freezing that uses treadmill
training associated with auditory and visual cues.
The aim of this study is to evaluate the efficacy of
our protocol and compare its results with those of a
traditional rehabilitation protocol using only auditory
and visual cues.
PATIENTS AND METHODS
Study Protocol
Forty patients with a diagnosis of ‘‘clinically proba-
ble’’ idiopathic Parkinson’s disease according to Gelb
et al.,11admitted to our hospital for rehabilitation treat-
ment, were enrolled into the study. The study was
approved by the local Ethical Committee and all subjects
gave their written informed consent before participation.
Inclusion criteria were: ability to walk without any
physical assistance, visual and hearing capacity suffi-
cient to perceive the cues, freezing of gait at the time
of peak medication effect ascertained by clinical exam-
ination, Hoehn-Yahr stage 3, no cognitive impairment
(mini-mental state examination score >26),12stable
pharmacological treatment.
Subjects were excluded if they had neurological con-
ditions other than idiopathic Parkinson’s disease, pos-
tural hypotension, cardiovascular disorders, musculo-
skeletal disorders, or vestibular dysfunction limiting
locomotion or balance.
The same neurologist examined the patients in the
morning, one hour after they had taken levodopa, at
baseline and at the end of the rehabilitation treatment.
Subjects were randomly assigned into two groups,
each composed of 20 patients. Patients in Group 1
underwent a rehabilitation protocol for gait disturbance
and freezing that used treadmill training associated
with auditory and visual cues. A motorized medical
treadmill (Locomotor Training, Biodex, IL) was used.
Subjects assigned to this group received training for 20
minutes every day for 4 weeks (28 sessions in all).
The patients were observed during treadmill training
by a physiatrist. Maximum tolerated walking speed
was determined before the training session. This speed
was reduced (240%) and used for a 2-day warm-up
period. After that, the belt speed was increased every
3 days by 0.05 stride cycles/second. During the train-
ing a visual cue and an auditory cue were used. The
visual cue was a target, displayed on a screen that the
patient had to reach with the stride. The shapes of right
and left feet were shown alternatively on the screen.
When the patient’s stride fell within the set standard
deviation (SD), the footfalls were synchronized with
the target shapes and ‘‘well done’’ appeared on the
screen. When the stride fell outside the SD, the foot-
falls and target shapes were out of synchronization and
the patient was informed, on the screen, of which foot-
fall was outside of the SD and prompted to take a lon-
ger or shorter step with the respective foot. The audi-
tory cue consisted of musical beats synchronized with
the visual cues with a frequency of 0.5 c/s.
Patients in Group 2 followed a traditional rehabilita-
tion protocol using only auditory and visual cues. Sub-
jects assigned to this group also received training for
20 minutes every day for 4 weeks (28 sessions in all).
The visual cue used during the gait training in this
group consisted of lines spaced according to individual
stride length. These lines were separated by a further
0.05 m per stride every 3/4 days. The auditory cue was
a musical beat with the same frequency as that used
for Group 1 (0.5 c/s).
The rating scales used for the clinical evaluation
were the Unified Parkinson’s Disease Rating Scale
Motor Section (UPDRS III)13and the Freezing of Gait
Questionnaire (FOGQ),14which is compiled by the
same neurologist at the start and at the end of the reha-
bilitation program.
Gait was assessed by meters walked during a 6-mi-
nute walking test (6MWT), gait speed and stride
length. All measurements were performed at the start
and at the end of the rehabilitation program. The 6-mi-
nute walking test was conducted following a standar-
dized procedure: the patient was first familiarized with
the test by letting him/her go once forward and back-
ward along a straight 30-m line on the level in a gym-
nasium. Then, after 15 minutes rest, he/she was
instructed to walk from end to end of the line for 6
minutes and to cover as much distance as possible. No
encouragement was offered during the test and no cues
were used.
The gait speed and stride length were evaluated
using the motorized medical treadmill endowed with
four strain gauges under the belt sensitive to the bend-
ing of the belt itself caused by the weight applied by
the patient walking. These gauges are connected to
software that enables an evaluation of the various pa-
rameters under investigation. All patients were fami-
liarized with the motorized treadmill before performing
the evaluation at the start of the rehabilitation program,
while only patients from Group 2 were again familiar-
ized with the treadmill before performing the evalua-
tion at the end of the rehabilitation program. The gait
1140 G. FRAZZITTA ET AL.
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speed and stride length of the patients in both groups
were evaluated without the use of cues.
Statistical Analysis
Shapiro–Wilk statistic was used to test the normality
of the distribution of all variables.
The effect of the rehabilitation strategy on each clin-
ical variable considered was assessed by a two factor
analysis of variance: training program (treadmill versus
traditional treatment) and time (end of treatment versus
baseline), with repeated measures in the time factor.
Within-group comparisons were carried out by
paired t-test or by Wilcoxon’s matched pairs test in
case of violation of the normality assumption. Between
group comparisons were carried out by unpaired T-test
or by Mann–Whitney U-test if appropriate. Descriptive
statistics are given as mean 6 SD. A P value <0.05
was considered statistically significant.
All analyses were carried out using the SAS/STAT
statistical package, release 8.02 (SAS Institute Inc.,
Cary, NC).
RESULTS
There were no drop outs and compliance was good
and comparable in both groups.
The demographic and clinical characteristics of
Group 1 and Group 2 patients, at baseline and after the
rehabilitation program, are reported in Table 1. No
statistically significant differences
between the two groups in any variable at baseline.
The performance of both groups of patients improved
significantly by the end of the training program. How-
ever, the results achieved by the treadmill treatment
(Group 1) were better than those of the traditional
rehabilitation protocol (Group 2).
Results from repeated measurements analysis of var-
iance confirmed the overall improvement of all clinical
wereobserved
variables in both groups, and showed significant time-
treatment effect in favor of the patients in Group 1 in
most considered variables (P 5 0.007, P 5 0.0004, P
5 0.0126, and P 5 0.0263 for FOGQ scores, 6MWT,
gait speed, and stride cycle, respectively). No statisti-
cally significant time-treatment effect was observed for
UPDRS III score (P 5 0.1466).
Figure 1 is a graphical representation of these results
for 6MWT, FOGQ, gait speed, and stride cycle. Differ-
ences in treatment effect on a given clinical indicator
are reflected by differences in the slope of the lines
joining the mean value of the clinical indicator at the
baseline and after treatment in the two groups.
DISCUSSION
In this study of patients with Parkinson’s disease
who underwent two different types of rehabilitation
programs, both groups of patients showed a significant
improvement of gait and freezing after the rehabilita-
tion treatment. These results are in agreement with
those of previous studies on the use of rehabilitation
protocols for gait.10,15-18However, patients treated
with treadmill training and auditory and visual cues
(Group 1) had better results at the end of treatment. In
particular, patients in Group 1 showed statistically sig-
nificant better improvements in FOGQ score, distance
walked in the 6-minute walking test, gait speed and
stride cycle.
Parkinson’s disease is due to a depletion of dopa-
mine production in neurons in the basal ganglia of the
brain and patients have a disorder in sensory-motor
integration.19Basal ganglia control the ability to per-
form well learned motor skills, such as walking and
turning around, by sending to the cerebral cortex cues
and sets able to regulate the speed and amplitude of
movements.20,21Because of an imbalance of neuro-
transmitters in the brain, people with Parkinson’s dis-
TABLE 1. Demographic and clinical characteristics of the patients in Group 1 and Group 2, at baseline and after the
rehabilitation program
Group 1 baseline Group 2 baselineGroup 1 after trainingGroup 2 after training
Age
Duration of the disease (yr)
Male/female
Levodopa (mg)
UPDRS III score
FOGQ score
6MWT (m)
Speed (m/S)
Stride cycle (cycle/S)
71 (8)
13.2 (4.1)
8/12
685 (246)
21.6 (5.6)
11.6 (3.0)
221 (89)
0.6 (0.2)
0.6 (0.2)
71 (7)
12.9 (4.6)
9/11
720 (232)
23.6 (5.2)
11.4 (2.4)
226 (70)
0.5 (0.1)
0.6 (0.1)
14.5 (3.7)*
6.5 (1.9)*
351 (125)*
1.0 (0.3)*
0.8 (0.2)*
17.8 (4.3)*
7.7 (1.8)*
283 (77)*
0.8 (0.2)*
0.7 (0.1)*
The data are expressed in mean (SD).
*P ? 0.0001 compared with baseline.
1141REHABILITATION TREATMENT OF FREEZING
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ease progressively lose flexibility and adaptability in
their locomotor responses and walk with a stereotypi-
cal short-stepped, narrow-based shuffling gait. They
also experience difficulty in modulating gait parameters
in response to tasks demanding changes.22Freezing
may be a manifestation of a problem with maintenance
of the internal gait rhythm.16,23
The efficacy of auditory and visual cues in rehabili-
tation treatment of gait disorders in Parkinson’s
patients is well known.4,16,24The auditory cues provide
an external rhythm, which is able to compensate for
the defective internal rhythm of the basal ganglia.25
People with Parkinson’s disease do not lose the ability
to generate a healthy stepping pattern, but have diffi-
culty in activating the motor control system. Visual
cues help to fill in for the motor set deficiency by pro-
viding visual data on appropriate stride length.21The
visual cues generate an optical flow that may activate
a cerebellar visual-motor pathway.26
In addition, it has been shown that treadmill training
is effective in reducing falls and improving gait parame-
ters in patients with Parkinson’s disease.16,17Finally,
Herman and Frenkel-Toledo hypothesize that treadmill
training also acts as an external cue, setting the walking
pattern and reinforcing neuronal circuits that contribute
to gait pacing.8,27Several researchers have reported that
treadmill training is effective in improving mobility8-10
and Miyai hypothesized that cortical reorganization,
especially in the supplementary motor area, might be a
possible mechanism underlying the improvement.18
Our data suggest that treadmill training associated
with auditory and visual cues can be more effective
than conventional treatment with auditory and visual
cues alone. Treadmill training probably imposes exter-
nal pace and focuses attention on gait. In this sense it
might act as a supplementary external cue able to
improve the efficacy of the traditional auditory and vis-
ual cues.27
FIG. 1.
and stride cycle (bottom right). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]
Graphical representation of time-treatment interaction for the variables 6MWT (top left), FOGQ (top right), gait speed (bottom left),
1142G. FRAZZITTA ET AL.
Movement Disorders, Vol. 24, No. 8, 2009

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Study Limitations
This study considered only the acute effect of the
treadmill rehabilitation protocol, but whether the treat-
ment has prolonged clinical efficacy without the need
to change pharmacological treatment remains unex-
plored. Future studies following a group of patients
treated with treadmill training for a suitable period is
devised to assess the long-term effects of this rehabili-
tation protocol.
Finally, it may be questioned whether the better
improvement in patients treated with treadmill may be
due to the habituation to treadmill walking. We used
the software of the motorized treadmill only to evalu-
ate gait speed and stride cycle. It should be noted that
the patients treated with treadmill training and auditory
and visual cues had better results at the end of treat-
ment with significant improvements also in FOGQ
score and that the functional indicator which showed
the most impressive improvement was the distance
walked in the 6-minute walking test, a result which
cannot be attributed to habitual use of a treadmill.
Hence, we think that habituation to treadmill walking
did not play a relevant role in our results and their
interpretation.
Acknowledgment: This work was supported by grants
from the S. Maugeri Foundation IRCCS (Istituto di Ricovero
e Cura a Carattere Scientifico), Ricerca Corrente, 2007. We
thank Rachel Stenner and Furione Milena for their assistance.
Author Roles: Giuseppe Frazzitta: Research project: Con-
ception and organization. Manuscript: Writing of the first draft;
Roberto Maestri: Statistical analysis: Design and execution.
Manuscript: Review and critique; Davide Uccellini: Research
project: Organization; Gabriella Bertotti: Research project:
Execution; Paola Abelli: Research project: Organization.
REFERENCES
1. Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM,
Giladi M. Characterization of freezing of gate subtypes and
response of each to levodopa in Parkinson’s disease. Eur J Neu-
rol 2003;10:391–398.
2. Poewe W, Granata R. Pharmacological treatment of Parkinson’s
disease. In: Watts RL, Koller WC, editors. Movement disorders:
neurologic principles and practice. New York: McGraw-Hill;
1997. p 201–219.
3. Fernandez del Olmo M, Cudeiro J. A simple procedure using au-
ditory stimuli to improve movement in Parkinson’s disease: a
pilot study. Neurol Clin Neurophysiol 2003;25:2003–2022.
4. Rochester L, Hetherington V, Jones D, Nieuwboer A, Willems
AM, Kwakkel G, Van Wegen E. The effect of external rhythmic
cues (auditory and visual) on walking during a functional task in
homes of people with Parkinson’s disease. Arch Phys Med Reha-
bil 2005;86:999–1006.
5. del Olmo MF, Cudeiro J. Temporal variability of gait in Parkin-
son disease: effects of a rehabilitation programme based on
rhythmic sound cues. Parkinsonism Rel Disord 2005;11:25–33.
6. Sidaway B, Anderson J, Danielson G, Martin L, Smith G. Effects
of long-term gait training using visual cues in an individual with
Parkinson disease. Phys Ther 2006;86:186–194.
7. Jiang Y, Norman K. Effects of visual and auditory cues on gait
initiation in people with Parkinson’s disease. Clin Rehabil
2006;20:36–45.
8. Herman T, Giladi N, Gruendlinger L, Hausdorff JM. Six weeks
of intensive treadmill training improves gait and quality of life in
patients with Parkinson’s disease: a pilot study. Arch Phys Med
Rehabil 2007;88:1154–1158.
9. Cakit BD, Saracoglu M, Genc H, Erdem HR, Inan L. The effects
of incremental speed-dependent treadmill training on postural
instability and fear of falling in Parkinson’s disease. Clin Rehabil
2007;21:698–705.
10. Pohl M, Rockstroh G, Ruckriem S, Mrass G, Mehrholz J. Imme-
diate effects of speed-dependent treadmill training on gait param-
eters in early Parkinson’s disease. Arch Phys Med Rehabil
2003;84:1760–1766.
11. Gelb DJ, Oliver E, Gilman S. Diagnostic criteria for Parkinson
disease. Arch Neurol 1999;56:33–39.
12. Folstein M, Folstein S, McHugh P. ‘‘Mini-mental state’’ a practi-
cal method for grading the cognitive state of patients for the cli-
nician. J Psychiatr Res 1975;12:189–198.
13. Fahn S, Elton RL. Unified Parkinson’s disease rating scale. In:
Fahn S, Marsden CD, Calne D, Goldstein M, editors. Recent
developments in Parkinson’s disease. Florham Park, NJ: Macmil-
lan Health Care Information; 1987. p 153–164.
14. Giladi N, Shabtai H, Simon ES, Biran S, Tal J, Korczyn AD.
Construction of freezing of gait questionnaire for patients with
parkinsonism. Parkinsonism Relat Disord 2000;6:165–170.
15. Brichetto G, Pelosin E, Marchese R, Abbruzzese G. Evaluation
of physical therapy in parkinsonian patients with freezing of gait:
a pilot study. Clin Rehabil 2006;20:31–35.
16. Rubinstein TC, Giladi N, Hausdorff JM. The power of cueing to
circumvent dopamine deficits: a review of physical therapy treat-
ment of gait disturbance in Parkinson’s disease. Mov Disord
2002;17:1148–1160.
17. Protas EJ, Mitchell K, Williams A, Quereshy H, Caroline K, Lai
EC. Gait and step training to reduce falls in Parkinson’s disease.
Neuro Rehabil 2005;20:183–190.
18. Miyai I, Fujimoto Y, Ueda Y, Yamamoto H, Nozaki S, Saito T,
Kang J. Treadmill training with body weight support: its effect
on Parkinson’s disease. Arch Phys Med Rehabil 2000;81:849–
852.
19. Abbruzzese G, Berardelli A. Sensorimotor integration in move-
ment disorders. Mov Disord 2003;18:231–240.
20. Cunnington R, Jansek R, Bradshaw JL, Phillips JG. Movement-
related potentials in Parkinson’s disease. Presence and predict-
ability of temporal and spatial cues. Brain 1995;118:935–950.
21. Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length
regulation in Parkinson’s disease. Normalization strategies and
underlying mechanisms. Brain 1996;119:551–568.
22. Morris ME, Huxham F, McGinley J, Dodd K, Iansek R. Review:
the biomechanics and motor control of gait in Parkinson disease.
Clin Biomech 2001;16:459–470.
23. Okuma Y. Freezing of gait in Parkinson’s disease. J Neurol
2006;253:27–32.
24. Lim I, Van Wegen E, de Goede C, et al. Effects of external
rhythmical cueing on gait in patients with Parkinson’s disease: a
systematic review. Clin Rehabil 2005;19:695–713.
25. McIntosh GC, Brown SH, Rice RR, et al. Rhythmic auditory-
motor facilitation of gait patterns in patients with Parkinson’s
disease. J Neurol Neurosurg Psychiatry 1997;62:22–26.
26. Azulay JP, Masure S, Amblard B, et al. Visual control of loco-
motion in Parkinson’s disease. Brain 1999;122 (Part 1):111–120.
27. Frenkel-Toledo S, Giladi N, Peretz C, Herman T, Gruendlinger
L, Hausdorff M. Treadmill walking as an external pacemaker to
improve gait rhythm and stability in Parkinson’s disease. Mov
Disord 2005;20:1109–1114.
1143 REHABILITATION TREATMENT OF FREEZING
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